During visual search, the working memory (WM) representation of the search target guides attention to matching items in the visual scene. However, we can hold multiple items in WM. Do all these items guide attention at the same time? Using a new functional magnetic resonance imaging visual search paradigm, we found that items in WM can attain two different states that influence activity in extrastriate visual cortex in opposite directions: whereas the target item in WM enhanced processing of matching visual input, other “accessory” items in memory suppressed activity. These results imply that the representation of task-relevant and (currently) task-irrelevant representations in WM differs, revealing new insights into the organization of human visual WM. The suppressive influence of irrelevant WM items may complement the attention-guiding influence of task-relevant WM items, helping us to focus on task-relevant information without getting distracted by irrelevant memory content.